Human Infection with MERS Coronavirus after Exposure to Infected Camels, Saudi Arabia, 2013
Human Infection with MERS Coronavirus after Exposure to Infected Camels, Saudi Arabia, 2013

Ziad A. Memish, Matthew Cotten, Benjamin Meyer, Simon J. Watson, Abdullah J. Alsahafi, Abdullah A. Al Rabeeah, Victor Max Corman, Andrea Sieberg, Hatem Q. Makhdoom, Abdullah Assiri, Malaki Al Masri, Souhaib Aldabbagh, Berend-Jan Bosch, Martin Beer, Marcel A. Müller, Paul Kellam, and Christian Drosten

Author affiliations: Al Faisal University, Riyadh, Saudi Arabia (Z.A. Memish); Global Centre for Mass Gatherings Medicine, Riyadh (Z.A. Memish, A.A. Al Rabeeh); Ministry of Health, Riyadh (Z.A. Memish, A.A. Al Rabeeh, A. Assiri, M. Al Masri); Wellcome Trust Sanger Institute, Hinxton, UK (M. Cotten, S.J. Watson, P. Kellam);University of Bonn Medical Centre Institute of Virology, Bonn, Germany (B. Meyer, V.M. Corman, A. Sieberg, S. Aldabbagh, M.A. Müller, C. Drosten); Regional Health Directorate, Jeddah, Saudi Arabia (A.J. Alsahafi); Jeddah Regional Laboratory, Jeddah (Hatem Q. Makhdoom); Utrecht University, the Netherlands (B.-J. Bosch);Friedrich-Loeffler-Institut, Institute for Virus Diagnostics, Greifswald–Insel Riems, Germany (M. Beer); University College London, London, UK (P. Kellam)

Abstract

We investigated a case of human infection with Middle East respiratory syndrome coronavirus (MERS-CoV) after exposure to infected camels. Analysis of the whole human-derived virus and 15% of the camel-derived virus sequence yielded nucleotide polymorphism signatures suggestive of cross-species transmission. Camels may act as a direct source of human MERS-CoV infection.

Middle East respiratory syndrome coronavirus (MERS-CoV) was identified in 2012 in a cell culture taken from a patient who died of pneumonia in Saudi Arabia (1). Since 2012, at least 187 laboratory-confirmed human cases of MERS-CoV infection, most resulting in respiratory tract illness, have been reported to the World Health Organization; 97 of these cases were fatal. Known cases have been directly or indirectly linked to countries in the Arabian Peninsula (2). Dromedary camels across and beyond the region show high rates of antibodies against MERS-CoV (3–7), and viral RNA has been detected in camels in different countries (8,9). In 1 instance, a camel and 2 humans caring for the camel were found to be infected with viruses that were highly similar but distinct within 4,395 nt of the camel-derived virus sequence, including several phylogenetically informative nucleotide changes (10). To investigate possible camel–human virus transmission, we analyzed an infection with MERS-CoV in a man after he had contact with an infected camel.

The Study

On November 3, 2013, the Ministry of Health of Saudi Arabia was notified of a suspected case of MERS-CoV infection in a 43-year-old male patient at King Abdulaziz University Hospital in Jeddah. The patient had cared for ill camels in his herd of 9 animals starting in early October, when the patient noted respiratory signs of illness with nasal discharge in several animals; he continued caring for the sick animals until October 27, the day of onset of his own illness. The patient cared for the animals for ≈3 hours per day 3 days per week, applying herbal remedies to the animals’ snouts and nostrils. He did not clean the stables or milk the animals, but he routinely consumed raw, unpasteurized camel milk from the herd.

Presence of MERS-CoV RNA in the patient was confirmed at Jeddah Regional Laboratory by using reverse transcription PCR (RT-PCR) targeting the upE and orfA gene fragments (11,12). Respiratory swab specimens yielded detectable signal after 28 RT-PCR cycles, indicative of an approximate viral load of 350,000 RNA copies per sample. A nearly complete viral genome was obtained (Jeddah_1_2013; GenBank accession no. KJ556336), confirming the presence of a typical MERS-CoV whose closest relatives were in the Riyadh_3 clade, as defined in (2) (phylogeny shown in online Technical Appendix

[PDF - 442 KB - 3 pages] Figure 1,wwwnc.cdc.gov/EID/article/20/6/14-0402-Techapp1.pdf

[PDF - 442 KB - 3 pages]).

To identify potential sources of infection, on November 9, the Ministry of Health investigated 5 close household contacts and the animal attendant on a farm owned by the patient. Nasopharyngeal swab samples were taken and tested at Jeddah Regional Laboratory by using RT-PCR. Deep nasal swab specimens were taken on the same day from 3 of the 9 camels at the farm. Testing of all samples by RT-PCR using the upE assay (11,12) did not detect MERS-CoV RNA in any of the human patients, but 1 of the 3 camels (camel G) tested positive (cycle threshold [C_t] = 33). On November 13, nasal swab samples were obtained from all 9 animals.upE RT-PCR results were positive for camel G (C_t = 38) and a second camel (camel B; C_t = 39).

Samples from November 13 and a small remaining amount of RNA extract from camel G from November 9 were sent to the Sanger Institute in Cambridge, UK, and confirmation of reactivity (C_t ≈ 38) was obtained for pooled samples with the upE assay from camel G but not for camel B. The result for camel G was confirmed at the Institute of Virology in Bonn, Germany, for the same samples by using real-time RT-PCRs targeting the upE and 1A diagnostic target regions.

Dr Memish is Deputy Minister for Public Health, Ministry of Health; director of the WHO Collaborating Center for Mass Gathering Medicine; and professor at Alfaisal University College of Medicine, Riyadh, Kingdom of Saudi Arabia. His research interest is MERS coronavirus.

Acknowledgment

The work was funded by the European Community’s Seventh Framework Programme (FP7/2007–2013) under the project EMPERIE, European Community grant agreement number 223498 and ANTIGONE, contract number 278976. C.D. has received infrastructural support from the German Centre for Infection Research.

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Suggested citation for this article: Memish ZA, Cotton M, Meyer B, Watson SJ, Alsahafi AJ, Al Rabeeah AA, et al. Human infection with MERS coronavirus after exposure to infected camels, Saudi Arabia, 2013. Emerg Infect Dis [Internet]. 2014 Jun [date cited].http://dx.doi.org/10.3201/eid2006.140402